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Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh

Wilbanks, Elizabeth G. and Jaekel, Ulrike and Salman, Verena and Humphrey, Parris T. and Elsen, Jonathan A. and Facciotti, Marc T. and Buckley, Daniel H. and Zinder, Stephen H. and Druschel, Gregory K. and Fike, David A. and Orphan, Victoria J. (2014) Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh. Environmental Microbiology, 16 (11). pp. 3398-3415. ISSN 1462-2912. PMCID PMC4262008. https://resolver.caltech.edu/CaltechAUTHORS:20150107-070238329

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Abstract

Microbial metabolism is the engine that drives global biogeochemical cycles, yet many key transformations are carried out by microbial consortia over short spatiotemporal scales that elude detection by traditional analytical approaches. We investigate syntrophic sulfur cycling in the ‘pink berry’ consortia of the Sippewissett Salt Marsh through an integrative study at the microbial scale. The pink berries are macroscopic, photosynthetic microbial aggregates composed primarily of two closely associated species: sulfide-oxidizing purple sulfur bacteria (PB-PSB1) and sulfate-reducing bacteria (PB-SRB1). Using metagenomic sequencing and ^(34)S-enriched sulfate stable isotope probing coupled with nanoSIMS, we demonstrate interspecies transfer of reduced sulfur metabolites from PB-SRB1 to PB-PSB1. The pink berries catalyse net sulfide oxidation and maintain internal sulfide concentrations of 0–500 μm. Sulfide within the berries, captured on silver wires and analysed using secondary ion mass spectrometer, increased in abundance towards the berry interior, while δ^(34)S-sulfide decreased from 6‰ to −31‰ from the exterior to interior of the berry. These values correspond to sulfate–sulfide isotopic fractionations (15–53‰) consistent with either sulfate reduction or a mixture of reductive and oxidative metabolisms. Together this combined metagenomic and high-resolution isotopic analysis demonstrates active sulfur cycling at the microscale within well-structured macroscopic consortia consisting of sulfide-oxidizing anoxygenic phototrophs and sulfate-reducing bacteria.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1111/1462-2920.12388DOIArticle
http://onlinelibrary.wiley.com/doi/10.1111/1462-2920.12388/abstractPublisherArticle
http://onlinelibrary.wiley.com/doi/10.1111/1462-2920.12388/suppinfoPublisherSupporting Information
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4262008/PubMed CentralArticle
ORCID:
AuthorORCID
Fike, David A.0000-0003-2848-0328
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2014 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Received 7 November, 2013; revised 30 December, 2013; accepted 5 January, 2014. We would like to acknowledge the excellent work of many students, teaching fellows, and instructors who contributed to this research over the many years of the Microbial Diversity course at the Marine Biological Laboratory; in particular we thank Cristina Moraru and Rebekah J. Ward for assistance in developing embedding and CARD-FISH protocols, Jarrod J. Scott for providing 16S rRNA gene sequence data from 2007 and Alexander P. Petroff for helpful discussions. Many thanks to Douglas C. Nelson and Susan E. Alford for their work with the radiocarbon fixation assay, Abigail Green-Saxena and Yunbin Guan for assistance with nanoSIMS data acquisition, Fotios C. Kafantaris for microvoltammetry work, Jennifer Houghton Julie Huber for use of her lab and Claire Beaudoin for sulfide microsensors measurements, and to Nanelle R. Barash and Annette R. Rowe for their critical reading of the manuscript. This work was supported by NSF grants DEB-1310168, EAR-1124389, and EAR-1123391, a grant from the Gordon and Betty Moore Foundation (#3306), and awards to Elizabeth G. Wilbanks from the NSF Graduate Research Fellowship, UC Davis Dissertation Year Fellowship, P.E.O. Scholar Award, and the NAI/APS Lewis and Clark Fund in Astrobiology. This research was performed by participants in the MBL Microbial Diversity course and was supported in part by the Howard Hughes Medical Foundation, the Gordon and Betty Moore Foundation (#2493), the NSF (DEB-0917499), the US DOE (DEFG02-10ER13361), and the NASA Astrobiology Institute.
Funders:
Funding AgencyGrant Number
NSFDEB-1310168
NSFEAR-1124389
NSFEAR-1123391
Gordon and Betty Moore Foundation3306
NSF Graduate Research FellowshipUNSPECIFIED
UC Davis Dissertation Year Fellowship, P.E.O. Scholar AwardUNSPECIFIED
NAI/APS Lewis and Clark Fund in AstrobiologyUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore Foundation2493
NSFDEB-0917499
Department of Energy (DOE)DE-FG02-10ER13361
NASAUNSPECIFIED
Issue or Number:11
PubMed Central ID:PMC4262008
Record Number:CaltechAUTHORS:20150107-070238329
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20150107-070238329
Official Citation:Wilbanks, E. G., Jaekel, U., Salman, V., Humphrey, P. T., Eisen, J. A., Facciotti, M. T., Buckley, D. H., Zinder, S. H., Druschel, G. K., Fike, D. A. and Orphan, V. J. (2014), Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh. Environmental Microbiology, 16: 3398–3415. doi: 10.1111/1462-2920.12388
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:53247
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:07 Jan 2015 17:07
Last Modified:13 Dec 2019 00:43

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